Dynamics of Leishmania Infection Rates in Rhombomys Opimus
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Bull. Soc. Pathol. Exot. DOI 10.1007/s13149-010-0044-1 EPIDEMIOLOGY / EPIDÉMIOLOGIE Dynamics of Leishmania infection rates in Rhombomys opimus (Rodentia: Gerbillinae) population of an endemic focus of zoonotic cutaneous leishmaniasis in Iran Dynamique des taux d’infection à Leishmania chez les populations de Rhombomys opimus (Rodentia : Gerbillinae) dans un foyer endémique de leishmaniose cutanée zoonotique en Iran A.A. Akhavan · M.R. Yaghoobi-Ershadi · A. Khamesipour · H. Mirhendi · M.H. Alimohammadian · Y. Rassi · M.H. Arandian · R. Jafari · H. Abdoli · N. Shareghi · M. Ghanei · N. Jalali-zand Received: 2 November 2009, Accepted: 23 December 2009 © Société de pathologie exotique et Springer-Verlag France 2010 Abstract Zoonotic cutaneous leishmaniasis (ZCL) due to reaction (PCR) assay was used for the detection and identi- Leishmania major is a great public health problem in the fication of Leishmania parasites, and the results were con- Old World. Leishmania major is widely distributed in popu- firmed by PCR–restriction fragment length polymorphism lations of rodents in arid and savannah regions. In this study, (RFLP). The results showed that Leishmania infection rate seasonal variation of natural infection with Leishmania para- was 55.8% (29 out of 52 gerbils) using nested PCR. The sites in Rhombomys opimus (Rodentia: Gerbillinae) popula- highest and lowest Leishmania infection rates were observed tion of an endemic focus of ZCL in Iran was monitored. The in fall and summer, respectively. Gerbils that were found to study was conducted from October 2007 to October 2008 in be infected only with L. major were 5.8%, and that with the central part of the country. Nested polymerase chain Leishmania turanica were 23.1%. A mixed natural infection was seen in the rodents with L. major and L. turanica (21.2%), with L. major and L. gerbilli (1.9%), and with all A.A. Akhavan · M.R. Yaghoobi-Ershadi (*) · Y. Rassi the three species (3.9%). Leishmania major infection alone Department of Medical Entomology and Vector Control, was seen in fall and winter whereas mixed infection of School of Public Health, Tehran University of Medical Sciences, L. major and L. turanica was observed in all seasons except Tehran, Iran in summer. Leishmania turanica infection was observed e-mail : [email protected] throughout the year. It is concluded that L. major, L. gerbilli, A. Khamesipour and L. turanica circulate in the population of R. opimus in Center for Research in Skin diseases and Leprosy, central part of Iran. Leishmania major infection is usually Tehran University of Medical Sciences, accompanied by L. turanica in naturally infected gerbils Tehran, Iran with the highest rate in fall. It is recommended that the role H. Mirhendi of L. turanica in the epidemiology and transmission of ZCL Department of Medical Parasitology and Mycology, should be reconsidered. School of Public Health, Tehran University of Medical Sciences, Tehran, Iran Keywords Rhombomys opimus · Leishmania major · L. gerbilli · L. turanica · Seasonal variation · Zoonotic M.H. Alimohammadian cutaneous leishmaniasis · Nested PCR · Badrood · Iran · Department of Immunology, Pasteur Institute of Iran, Middle South Asia Tehran, Iran M.H. Arandian · R. Jafari · H. Abdoli · N. Shareghi · M. Ghanei · Résumé La leishmaniose cutanée zoonotique (LCZ) due à N. Jalali-zand Leishmania major constitue un problème de santé publique Esfahan Training and Health Research Center, dans l’ancien monde. L. major est une espèce largement dis- National Institute of Health Research, Tehran University of Medical Sciences, tribuée dans les populations de rongeurs vivant dans les Esfahan, Iran régions arides et de savane. Dans la présente étude, la 2 Bull. Soc. Pathol. Exot. variation saisonnière de l’infection naturelle par les parasites Iran; Psammomys obesus (Fat Sand Rat) and Meriones cras- du genre Leishmania chez la Grande Gerbille Rhomb- sus in northern Africa and Middle East; and Tatera spp. in omys opimus (Rodentia: Gerbillinae) au sein d’une popula- subsaharan Africa and Iran [6]. R. opimus (Cricetidae: Gerbil- tion d’un foyer endémique de LCZ en Iran a été contrôlée. linae) is the principal L. major reservoir host in the vast terri- L’étude a été menée d’octobre 2007 à octobre 2008 dans la tory of the Turan lowland (west and south Kazakhstan and partie centrale de l’Iran. Une PCR nichée a été utilisée pour central Asia with adjacent parts of Afghanistan and Iran), la détection et l’identification du parasite Leishmania, et les Mongolia and, apparently, in some provinces of China. In résultats ont été confirmés par PCR-RFLP. Les résultats ont the Turan lowland, naturally infected R. opimus were reported montré que le taux d’infection par Leishmania était de from more than 200 places. The number of naturally infected 55,8 % (29 sur 52 animaux) en utilisant la PCR nichée. great gerbils showed to be greater than any other mammals Les taux d’infection par Leishmania les plus forts et les (other rodents, insectivores, and carnivores) [3]. plus faibles ont été observés, respectivement, en automne All the proven vectors of ZCL belong to the subgenus Phle- et en été ; 5,8 % des gerbilles étaient infectées par L. major botomus,i.e.Phlebotomus papatasi, the principal vector, and isolément et 23,1% par L. turanica isolément. Une infection related species: Phlebotomus salehi and Phlebotomus dubosqi. mixte naturelle a été observée chez les rongeurs associant Well-described stable ZCL systems are associated with L. major et L. turanica (21,2 %), ou associant L. major et L. major, Psammomys obesus,andPh. papatasi in North L. gerbilli (1,9 %), ou associant les trois espèces (3,9 %). Africa and Middle East and with R. opimus and Ph. papatasi L’infection due à L. major isolément a été observée en auto- in central Asia, Afghanistan, and Iran [6,19]. The distribution mne et en hiver. Une infection mixte associant L. major et and the role of rodents as reservoir hosts of ZCL are geograph- L. turanica a été observée en toutes saisons, sauf en été. ically specific in Iran. Rhombomys opimus is the main reser- L’infection à L. turanica a été observée tout au long de l’an- voir of ZCL in Central and North East (N.E.) Iran followed by née. En conclusion, les trois espèces L. major, L. gerbilli et M. libycus (Cricetidae: Gerbillinae), which is the primary res- L. turanica circulent dans la population de R. opimus dans la ervoir of ZCL in some areas of the central and southern Iran. In partie centrale de l’Iran. L. major est habituellement accom- the south and south west of the country, including the Iran– pagnée par L. turanica chez les gerbilles naturellement Iraq border, the reservoir rodent is Tatera indica, the Indian infectées avec un plus fort taux en automne. Le rôle de Jird (Cricetidae: Gerbillinae). In Baluchistan of Iran (border L. turanica dans l’épidémiologie et la transmission de la of Pakistan), M. hurrianae (Cricetidae: Gerbillinae) acts as a LCZ devrait être reconsidéré. reservoir host [7,8,12,13,18,22]. One of the major problems for the control and understanding of this neglected disease is Mots clés Rhombomys opimus · Leishmania major · the lack of information about the dynamics of Leishmania L. gerbilli · L. turanica · Variation saisonnière · parasites in rodent reservoir populations. In this study, sea- Leishmaniose cutanée zoonotique · PCR niche · Badrood · sonal variation of Leishmania species infection in Rhombomys Iran · Moyen-Orient opimus (Rodentia: Gerbillinae) population of an endemic focus in Central Iran was monitored. Introduction Materials and methods Zoonotic cutaneous leishmaniasis (ZCL), a neglected tropical Study area disease, is a public health problem with a clear and disturbing increase in the number of cases in some areas of the world The investigation was conducted over a period of 12 months [2,6]. Leishmania major is widely distributed in various from October 2007 to October 2008 in Badrood rural district populations of rodents in arid and savannah regions [6]. The (33° 42′ N, 52° 2′ E), 25 km from the city of Natanz, Natanz disease is endemic in many rural districts of Iran, in county, Esfahan Province, central Iran where ZCL is 17 provinces out of 30. Rodents belonging to subfamily Ger- endemic. Badrood district is located at an altitude of billinae are the main reservoir hosts of ZCL in Iran and other 1056 m, in the foothills of Karkas Mountains (altitude countries where ZCL is endemic [3,15,18]. Gerbils are the 3898 m) with a desert climate, hot summer and cold winter. most abundant mammals reported from natural ecosystems of Old World deserts [3]. Many rodent species act as reservoir Rodent collection hosts of ZCL: Rhombomys opimus (Great Gerbil) in central Asia, northern Afghanistan, and Iran; Meriones libycus Active colonies of gerbils in the district were identified and (Libyan Jird) in the Arabian Peninsula, central Asia, and the rodents were caught using approximately 40 Sherman Iran; Meriones hurrianae (Indian Desert Jird) in India and traps baited with cucumber, in different seasons. In spring Bull. Soc. Pathol. Exot. 3 to fall, the traps were placed at the gerbil holes in the after- were visualized by agarose gel electrophoresis and ethidium noon and were collected in the morning on the following bromide staining. The identity of all species identified by day. In winter, Sherman traps were placed after sunrise and nested PCR was confirmed based on species-specific pattern were collected at noon on the same day. The trapped gerbils of PCR-RFLP using the restriction digestion with MnlI. were transferred to the animal house facility at the Esfahan Digestion was performed by adding 5 U (0.5 μl of the Training and Health Research Center, National Institute of enzyme) and 1.5 μl of the relevant buffer to a 13 μl aliquot Health, Esfahan, Iran, and maintained until use for parasito- of the nested PCR product in a final volume of 15 μl.